Chemoecology

, Volume 23, Issue 1, pp 45–57 | Cite as

The multifunctional pygidial gland secretion of the Steninae (Coleoptera: staphylinidae): ecological significance and evolution

  • Andreas Schierling
  • Karlheinz Seifert
  • Sebastian R. Sinterhauf
  • Julian B. Rieß
  • Johanna C. Rupprecht
  • Konrad Dettner
Research Paper

Abstract

The pygidial gland secretion of the rove beetle genera Stenus Latreille and Dianous Leach is composed of pyridine and piperidine-derived alkaloids and several terpene compounds. Two-choice bioassays with ants and fish, as well as agar diffusion assays, revealed that the secretion compounds are capable of deterring predators and protecting the beetles from infestation with microorganisms. In addition, the beetles use the secretion for rapid movements on the water surface, a process called skimming. Thus, originally developed to chemically defend the sensitive unprotected abdomen from predator attacks, the secretion of recent Steninae can be designated as multifunctional. Four of the alkaloid compounds occur as different configurational isomers in the secretion. Two-choice tests showed that ants discriminate between stereoisomers of stenusine, while there was no effect visible on bacteria in agar diffusion assays. Furthermore, there are evolutionary trends within the Steninae concerning the secretion composition, as some of the alkaloids primarily occur in phylogenetically basal species, while others are mainly restricted to derived species.

Keywords

Steninae Alkaloids Terpenes Deterrent Antibiotic Antifungal Evolution 

Notes

Acknowledgments

We would like to thank T. Müller (group of K. Seifert) for providing us with the secretion alkaloids as well as V. Puthz (Castle Museum Schlitz, Germany) for help with the identification of species and numerous helpful hints concerning Stenus phylogeny. L. Koerner and O. Betz (University of Tübingen) is thanked for molecular phylogeny data and J. Woodring (University of Bayreuth) for correcting the English of the manuscript. Support for this research by a grant from the German Research Foundation (DFG) (SE-595/14-1 and DE 258/12-1) is gratefully acknowledged.

References

  1. Andrews JM (2005) BSAC standardized disc susceptibility testing method (Version 4). J Antimicrob Chemother 56:60–76PubMedCrossRefGoogle Scholar
  2. Assing V, Puthz V (1998) 55. Gattung: Stenus Latreille. In: Lucht W, Klausnitzer, B (eds) Die Käfer Mitteleuropas, vol 15. Gustav Fischer, Jena, pp 130–131Google Scholar
  3. Benfield EF (1972) A defensive secretion of Dineutes discolour (Coleoptera: Gyrinidae). Ann Entomol Soc Am 65:1324–1327Google Scholar
  4. Betz O (1996) Function and evolution of the adhesive prey capture apparatus of Stenus species (Coleoptera, Staphylinidae). Zoomorpholgy 116:15–34CrossRefGoogle Scholar
  5. Betz O (1998) Life forms and hunting behavior of some Central European Stenus species (Coleoptera, Staphylinidae). Appl Soil Ecol 9:96–74Google Scholar
  6. Betz O (1999) A behavioral inventory of adult Stenus species (Coleoptera: Staphylinidae). J Nat Hist 33:1691–1712CrossRefGoogle Scholar
  7. Billard G, Bruyant C (1905) Sur une mode particulier de locomotion de certains Stenus. CR Soc Biol 59:102–103Google Scholar
  8. Blum MS (1981) Chemical defenses of arthropods. Academic Press, New YorkGoogle Scholar
  9. Deml R, Dettner K (1995) “Balloon hairs” of gipsy moth larvae (Lep., Lymantriidae): morphology and comparative chemistry. Comp Biochem Physiol 112B:673–681Google Scholar
  10. Dettner K (1985) Ecological and phylogenetic significance of defensive compounds from pygidial glands of Hydradephaga (Coleoptera). Proc Acad Natl Sci Phila 137:156–171Google Scholar
  11. Dettner K (1987) Chemosystematics and evolution of beetle chemical defense. Annu Rev Entomol 32:17–48CrossRefGoogle Scholar
  12. Dettner K (1991) Chemische Abwehrmechanismen bei Kurzflüglern (Coleoptera: Staphylinidae). Jber Naturwiss Ver Wuppertal 44:50–58Google Scholar
  13. Dettner K (1993) Defensive secretions and exocrine glands in free-living Staphylinid beetles—their bearing on phylogeny (Coleoptera: Staphylinidae). Biochem Syst Ecol 21:143–162CrossRefGoogle Scholar
  14. Dettner K, Scheuerlein A, Fabian P, Schulz S, Francke W (1996) Chemical defense of a giant springtail Tetrodontophora bielanensis (Waga) (Insecta: Collembola). J Chem Ecol 22:1051–1074CrossRefGoogle Scholar
  15. Eisner T, Aneshansley DJ (2000) Chemical defense: aquatic beetle (Dineutes hornii) vs. fish (Micropterus salmonides). Proc Natl Acad Sci USA 97:11313–11318PubMedCrossRefGoogle Scholar
  16. Eisner T, Meinwald J, Monro A, Ghent R (1961) Defence mechanisms of arthropods—I. The composition and function of the spray of the whipscorpion, Mastigoproctus giganteus (Lucas) (Arachnida, Pedipalpida). J Ins Physiol 6:272–298CrossRefGoogle Scholar
  17. Ekpa O, Wheeler JH, Cokendolpher JC, Duffield RM (1984) N,N-dimethyl-β-phenylamine and bornyl esters from the harvestman Sclerobunus robustus (Arachnida: Opiliones). Tetrahedron Lett 25:1315–1318CrossRefGoogle Scholar
  18. Francke W, Dettner K (2005) Chemical signaling in beetles. In: Schulz S (ed) Topics in current chemistry, vol 240. Springer, Heidelberg, pp 85–166Google Scholar
  19. Frey H (1973) Das Aquarium von A bis Z. Verlag J. Neumann-Neudamm, MelsungenGoogle Scholar
  20. Grebennikov VV, Newton AF (2009) Good-bye Scydmaenidae, or why the ant-like stone beetles should become megadiverse Staphylinidae sensu latissimo (Coleoptera). Eur J Entomol 106:275–301Google Scholar
  21. Herman LH (2001) Catalogue of the Staphylinidae (Insecta: Coleoptera). 1758 to the end of the second millennium. IV. Staphylininae group (Part 1). Bull Amer Mus Nat Hist 265:1807–2440Google Scholar
  22. Honda K (1983) Defensive potential of components of the larval osmeterial secretion of papilionid butterflies against ants. Physiol Entomol 8:173–179CrossRefGoogle Scholar
  23. Huth A, Dettner K (1990) Defense chemicals from abdominal glands of 13 rove beetle species of subtribe Staphylinina (Coleoptera: Staphylinidae, Staphylininae). J Chem Ecol 16:2691–2711CrossRefGoogle Scholar
  24. Jenkins MF (1957) The morphology and anatomy of the pygidial glands of Dianous coerulescens Gyllenhal (Coleoptera: Staphylinidae). Proc R Entomol Soc Lond 32:159–169Google Scholar
  25. Koch K (1989) Die Käfer Mitteleuropas. Ökologie, vol 1. Goecke and Evers, KrefeldGoogle Scholar
  26. Kohler P (1979) Die absolute Konfiguration des Stenusins und die Aufklärung weiterer Inhaltsstoffe des Spreitungsschwimmer Stenus comma. Dissertation, University of HeidelbergGoogle Scholar
  27. Kovac D, Maschwitz U (1989) Secretion-grooming in the water bug Plea minutissima: a chemical defence against microorganisms interfering with the hydrofuge properties if the respiratory region. Ecol Entomol 14:403–411CrossRefGoogle Scholar
  28. Kovac D, Maschwitz U (1990) Secretion-grooming in aquatic beetles (Hydradephaga): a chemical protection against contamination of the hydrofuge respiratory region. Chemoecology 1:131–138CrossRefGoogle Scholar
  29. Lang C, Seifert K, Dettner K (2012) Skimming behaviour and spreading potential of Stenus species and Dianous coerulescens (Coleoptera: Staphylinidae). Naturwissenschaften. doi: 10.1007/s00114-012-0975-4
  30. Leschen RAB, Newton AF (2003) Larval description, adult feeding behaviour, and phylogenetic placement of Megalopinus (Coleoptera: Staphylinidae). Coleopts Bull 57:469–493CrossRefGoogle Scholar
  31. Linsenmair KE (1963) Eine bislang unbekannte Fortbewegungsart bei Insekten: Das Entspannungsschwimmen. Kosmos 59:331–334Google Scholar
  32. Linsenmair KE, Jander R (1963) Das Entspannungsschwimmen von Velia und Stenus. Naturwissenschaften 50:231CrossRefGoogle Scholar
  33. Lohse GA (1964) Staphylinidae I (Micropeplinae bis Tachyporinae). In: Freude H, Harde KW, Lohse GA (eds) Die Käfer Mitteleuropas, vol 4. Goecke and Evers, KrefeldGoogle Scholar
  34. Lohse GA (1989) Ergänzungen und Berichtigungen zu Freude Harde Lohse “Die Käfer Mitteleuropas”. In: Lohse GA, Lucht W (eds) Die Käfer Mitteleuropas, vol 12. Goecke and Evers, Krefeld, pp 121–184Google Scholar
  35. Lusebrink I (2007) Stereoisomerie, Biosynthese und biologische Wirkung des Stenusins sowie weitere Inhaltsstoffe der Pygidialdrüsen der Kurzflüglergattung Stenus (Staphylinidae, Coleoptera). Dissertation, University of BayreuthGoogle Scholar
  36. Lusebrink I, Burkhardt D, Gedig T, Dettner K, Mosandl A, Seifert K (2007) Intrageneric differences in the four stereoisomers of stenusine in the rove beetle genus, Stenus (Coleoptera, Staphylinidae). Naturwissenschaften 94:143–147PubMedCrossRefGoogle Scholar
  37. Lusebrink I, Dettner K, Seifert K (2008a) Stenusine, an antimicrobial agent in the rove beetle genus Stenus (Coleoptera, Staphylinidae). Naturwissenschaften 95:751–755PubMedCrossRefGoogle Scholar
  38. Lusebrink I, Dettner K, Seifert K (2008b) Biosynthesis of stenusine. J Nat Prod 71:743–745PubMedCrossRefGoogle Scholar
  39. Lusebrink I, Dettner K, Schierling A, Müller T, Daolio C, Schneider B, Schmidt J, Seifert K (2009). New pyridine alkaloids from rove beetles of the genus Stenus (Coleoptera: Staphylinidae). Z Naturforsch 64c:271–278Google Scholar
  40. MacConnel JG, Blum MS, Fales HM (1971) The chemistry of fire ant venom. Tetrahedron 26:1129–1139CrossRefGoogle Scholar
  41. Maschwitz U (1967) Eine neuartige Form der Abwehr von Mikroorganismen bei Insekten. Naturwissenschaften 54:649PubMedCrossRefGoogle Scholar
  42. Morgan ED (2004) Biosynthesis in insects. RSC, CambridgeGoogle Scholar
  43. Mori K (1999) Miscellaneous natural products including marine natural products, pheromones, plant hormones, and aspects of ecology. In: Barton D, Nakanishi K, Meth-Cohn O (eds) Comprehensive natural product chemistry, vol 8. Elsevier, OxfordGoogle Scholar
  44. Müller T, Göhl M, Lusebrink I, Dettner K, Seifert K (2012) Cicindeloine from Stenus cicindeloides—isolation, structure elucidation and total synthesis. Eur J Org Chem 12:2323–2330Google Scholar
  45. Naomi S-I (1985) The phylogeny and higher classification of the Staphylinidae and their allied groups (Coleoptera, Staphylinoidae). Esakia 23:1–27Google Scholar
  46. Neumann S (1993) Die Analdrüsen der Spreitungsschwimmer (Coleoptera: Staphylinidae). Chemie und biologische Bedeutung. Diploma thesis at the Faculty of Biology, Chemistry and Geosciences, University of BayreuthGoogle Scholar
  47. Piffard A (1901) Steni gliding on the surface of water. Entomol Mon Mag 12:99Google Scholar
  48. Puthz V (1971) Revision der afrikanischen Steninenfauna und Allgemeines über die Gattung Stenus Latreille (Coleoptera, Staphylinidae). Ann Mus R Afr Centr Ser 8(187):1–376Google Scholar
  49. Puthz V (1974) Neue mexikanische Stenus-Arten: 135. Beitrag zur Kenntnis der Steninen (Coleoptera, Staphylinidae). Dtsch Entomol Z 21:203–216Google Scholar
  50. Puthz V (1981) Was ist Dianous Leach, 1819, was ist Stenus Latreille, 1796? Oder: Die Aporie des Stenologen und ihre taxonomischen Konsequenzen (Coleoptera: Staphylinidae) 180. Beitrag zur Kenntnis der Steninen. Entomol Abh Mus Tierk Dresden 44:87–132Google Scholar
  51. Puthz V (2006) Revision der neotropischen Stenus (Tesnus) Arten (Coleoptera: Staphylinidae) 288. Beitrag zur Kenntnis der Steninen. Rev Suisse Zool 113: 617-674 (with additional personal comments of V. Puthz)Google Scholar
  52. Puthz V (2008) Stenus Latreille und die segenreiche Himmelstochter (Coleoptera, Staphylinidae). Linzer biol Beitr 40:137–230Google Scholar
  53. Puthz V (2010) Stenus Latreille, 1797 aus dem baltischen Bernstein nebst Bemerkungen über andere fossile Stenus-Arten (Coleoptera, Staphylinidae) 313. Beitrag zur Kenntnis der Steninen. Ent Bl 106:265-287 (with additional personal comments of V. Puthz)Google Scholar
  54. Rödel HG, Coureaud G, Monclus R, Föhn S, Schaal B (2009) Abdominal odors of young, low-ranking European rabbit mothers are less attractive to pups: an experiment with animals living under natural breeding conditions. J Ethol 27:307–315CrossRefGoogle Scholar
  55. Schierling A, Schott M, Dettner K, Seifert K (2011) Biosynthesis of the defensive alkaloid (Z)-3-(2-methyl-1-butenyl)pyridine in Stenus similis beetles. J Nat Prod 74:2231–2234PubMedCrossRefGoogle Scholar
  56. Schierling A, Dettner K, Schmidt J, Seifert K (2012) Biosynthesis of the defensive alkaloid cicindeloine in Stenus solutus beetles. Naturwissenschaften 99:665–669PubMedCrossRefGoogle Scholar
  57. Schildknecht H (1970) The defensive chemistry of land and water beetles. Angew Chem Int Ed 9:1–9CrossRefGoogle Scholar
  58. Schildknecht H (1976) Chemical ecology—chapter of modern natural-products chemistry. Angew Chem Int Ed 15:214–222CrossRefGoogle Scholar
  59. Schildknecht H, Weis KH (1962) Zur Kenntnis der Pygidialblasensubstanzen vom Gelbrandkäfer (Dytiscus marginalis L.) XIII. Mitteilung über Insektenabwehrstoffe. Z Naturforsch 17B:448–452Google Scholar
  60. Schildknecht H, Krauss D, Connert J, Essenbreis H, Orfanides N (1975) The spreading alkaloid stenusine from the staphylinid Stenus comma (Coleoptera: Staphylinidae). Angew Chem Int Ed 14:427–427CrossRefGoogle Scholar
  61. Schildknecht H, Berger D, Krauss D, Connert J, Gelhaus J, Essenbreis H (1976) Defense chemistry of Stenus comma (Coleoptera: Staphylinidae). J Chem Ecol 2:1–11CrossRefGoogle Scholar
  62. Schoonhoven LM, van Loon JJA, Dicke M (2005) Insect plant biology, 2nd edn. Oxford University Press, OxfordGoogle Scholar
  63. Stoeffler M, Maier TS, Tolasch T, Steidle JML (2007) Foreign-language skills in rove-beetles? Evidence for chemical mimicry of ant alarm pheromones in myrmecophilous Pella beetles (Coleoptera: Staphylinidae). J Chem Ecol 33:1382–1392PubMedCrossRefGoogle Scholar

Copyright information

© Springer Basel 2012

Authors and Affiliations

  • Andreas Schierling
    • 1
  • Karlheinz Seifert
    • 2
  • Sebastian R. Sinterhauf
    • 1
  • Julian B. Rieß
    • 1
  • Johanna C. Rupprecht
    • 1
  • Konrad Dettner
    • 1
  1. 1.Institute of Animal Ecology II, University of BayreuthBayreuthGermany
  2. 2.Institute of Organic Chemistry, University of BayreuthBayreuthGermany

Personalised recommendations